Separating Recognition Processes of Declarative Memory via Anodal tDCS: Boosting Old Item Recognition by Temporal and New Item Detection by Parietal Stimulation

There is emerging evidence from imaging studies that parietal and temporal cortices act together to achieve successful recognition of declarative information; nevertheless, the precise role of these regions remains elusive. To evaluate the role of these brain areas in declarative memory retrieval, we applied bilateral tDCS, with anode over the left and cathode over the right parietal or temporal cortices separately, during the recognition phase of a verbal learning paradigm using a balanced old-new decision task. In a parallel group design, we tested three different groups of healthy adults, matched for demographic and neurocognitive status: two groups received bilateral active stimulation of either the parietal or the temporal cortex, while a third group received sham stimulation. Accuracy, discriminability index (d’) and reaction times of recognition memory performance were measurements of interest. The d’ sensitivity index and accuracy percentage improved in both active stimulation groups, as compared with the sham one, while reaction times remained unaffected. Moreover, the analysis of accuracy revealed a different effect of tDCS for old and new item recognition. While the temporal group showed enhanced performance for old item recognition, the parietal group was better at correctly recognising new ones. Our results support an active role of both of these areas in memory retrieval, possibly underpinning different stages of the recognition process.

[1]  R. Baayen,et al.  Mixed-effects modeling with crossed random effects for subjects and items , 2008 .

[2]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[3]  Hongkeun Kim,et al.  Trusting Our Memories: Dissociating the Neural Correlates of Confidence in Veridical versus Illusory Memories , 2007, The Journal of Neuroscience.

[4]  Daniel L. Schacter,et al.  ERP correlates of recognition memory: Effects of retention interval and false alarms , 2006, Brain Research.

[5]  Axel Mecklinger,et al.  ERP correlates of true and false recognition after different retention delays: stimulus- and response-related processes. , 2003, Psychophysiology.

[6]  Daniel L. Schacter,et al.  Suppressing False Recognition in Younger and Older Adults: The Distinctiveness Heuristic ☆ ☆☆ ★ , 1999 .

[7]  Alvaro Pascual-Leone,et al.  Temporal Lobe Cortical Electrical Stimulation during the Encoding and Retrieval Phase Reduces False Memories , 2009, PloS one.

[8]  V. Walsh,et al.  Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory , 2012, Brain Stimulation.

[9]  F. Strack,et al.  Memory for Nonoccurrences: Metacognitive and Presuppositional Strategies , 1994 .

[10]  M. Corbetta,et al.  Episodic Memory Retrieval, Parietal Cortex, and the Default Mode Network: Functional and Topographic Analyses , 2011, The Journal of Neuroscience.

[11]  L. Davachi,et al.  Behavioral/systems/cognitive Functional–neuroanatomic Correlates of Recollection: Implications for Models of Recognition Memory , 2022 .

[12]  Marcia K. Johnson,et al.  Source monitoring. , 1993, Psychological bulletin.

[13]  Brian A. Nosek,et al.  Power failure: why small sample size undermines the reliability of neuroscience , 2013, Nature Reviews Neuroscience.

[14]  A. Oeltermann,et al.  Hippocampal–cortical interaction during periods of subcortical silence , 2012, Nature.

[15]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[16]  D. Levy,et al.  Oppositional transcranial direct current stimulation (tDCS) of parietal substrates of attention during encoding modulates episodic memory , 2012, Brain Research.

[17]  Henrik Singmann,et al.  afex – Analysis of Factorial EXperiments , 2015 .

[18]  L. Squire,et al.  Structure and function of declarative and nondeclarative memory systems. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

[20]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[21]  John D E Gabrieli,et al.  Development of the declarative memory system in the human brain , 2007, Nature Neuroscience.

[22]  Daniel L. Schacter,et al.  Understanding metamemory: Neural correlates of the cognitive process and subjective level of confidence in recognition memory , 2006, NeuroImage.

[23]  M. Nitsche,et al.  Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans , 2001, Neurology.

[24]  Patrick S. R. Davidson,et al.  Does lateral parietal cortex support episodic memory? Evidence from focal lesion patients , 2008, Neuropsychologia.

[25]  Joseph Hilbe,et al.  Data Analysis Using Regression and Multilevel/Hierarchical Models , 2009 .

[26]  Michael Erb,et al.  Successful episodic memory retrieval of newly learned faces activates a left fronto-parietal network. , 2003, Brain research. Cognitive brain research.

[27]  E. Chua,et al.  Transcranial direct current stimulation (tDCS) of the parietal cortex leads to increased false recognition , 2015, Neuropsychologia.

[28]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[29]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[30]  P. Brockhoff,et al.  lmerTest: Tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package) , 2014 .

[31]  J. Jay Todd,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004, Nature.

[32]  Brice A. Kuhl,et al.  Neural Systems Underlying the Suppression of Unwanted Memories , 2004, Science.

[33]  Simon Dennis,et al.  ERP ‘old/new’ effects: memory strength and decisional factor(s) , 2002, Neuropsychologia.

[34]  Benjamin J. Shannon,et al.  Functional-Anatomic Correlates of Memory Retrieval That Suggest Nontraditional Processing Roles for Multiple Distinct Regions within Posterior Parietal Cortex , 2004, The Journal of Neuroscience.

[35]  Kenneth Hugdahl,et al.  A Standard Computerized Version of the Reading Span Test in Different Languages , 2008 .

[36]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[37]  John R. Anderson,et al.  Using model-based functional MRI to locate working memory updates and declarative memory retrievals in the fronto-parietal network , 2013, Proceedings of the National Academy of Sciences.

[38]  S. Ghetti Memory for nonoccurrences: The role of metacognition , 2003 .

[39]  A Baddeley,et al.  The fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Moscovitch,et al.  The parietal cortex and episodic memory: an attentional account , 2008, Nature Reviews Neuroscience.

[41]  Carlo Miniussi,et al.  Double dissociation of working memory load effects induced by bilateral parietal modulation , 2012, Neuropsychologia.

[42]  K. McDermott,et al.  Creating false memories: Remembering words not presented in lists. , 1995 .

[43]  Ingrid R. Olson,et al.  Dissociation Between Memory Accuracy and Memory Confidence Following Bilateral Parietal Lesions , 2009, Cerebral cortex.

[44]  Arne D. Ekstrom,et al.  Prestimulus theta activity predicts correct source memory retrieval , 2011, Proceedings of the National Academy of Sciences.

[45]  R. Buckner,et al.  Neural Correlates of Episodic Retrieval Success , 2000, NeuroImage.

[46]  G Buzsáki,et al.  The hippocampo-neocortical dialogue. , 1996, Cerebral cortex.

[47]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[48]  W. Sommer,et al.  Interplay of emotional valence and concreteness in word processing: An event-related potential study with verbs , 2013, Brain and Language.

[49]  Mark E Wheeler,et al.  Functional-anatomic correlates of remembering and knowing , 2004, NeuroImage.

[50]  John D E Gabrieli,et al.  The Development of Brain Systems Associated with Successful Memory Retrieval of Scenes , 2012, The Journal of Neuroscience.

[51]  Roberto Cabeza,et al.  Parietal Lobe and Episodic Memory: Bilateral Damage Causes Impaired Free Recall of Autobiographical Memory , 2007, The Journal of Neuroscience.

[52]  Marian E. Berryhill,et al.  Insights from neuropsychology: pinpointing the role of the posterior parietal cortex in episodic and working memory , 2012, Front. Integr. Neurosci..

[53]  V. Walsh,et al.  Short duration transcranial direct current stimulation (tDCS) modulates verbal memory , 2012, Brain Stimulation.

[54]  L. Squire Memory systems of the brain: A brief history and current perspective , 2004, Neurobiology of Learning and Memory.

[55]  John T Wixted,et al.  In defense of the signal detection interpretation of remember/know judgments , 2004, Psychonomic bulletin & review.

[56]  S. Houle,et al.  Activation of medial temporal structures during episodic memory retrieval , 1996, Nature.

[57]  A. Baddeley Recent developments in working memory , 1998, Current Opinion in Neurobiology.